Sall1 regulates cortical neurogenesis and laminar fate specification in mice: Implications for neural abnormalities in Townes-Brocks syndrome

DMM Disease Models and Mechanisms

Volumn 5, Issue 3, 2012, Pages 351-365

  Harrison, Susan J ^a,b,e   Nishinakamura, Ryuichi ^c   Jones, Kevin R ^d   Monaghan, A Paula ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c KUMAMOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SALL1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SIZE; BRAIN STEM CELL; CELL COUNT; CELL CYCLE; CELL DEATH; CELL MATURATION; GENE MUTATION; IMMUNOHISTOCHEMISTRY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; THALAMUS INTRALAMINAR NUCLEUS; TOWNES BROCKS SYNDROME;

ABNORMALITIES, MULTIPLE; ANIMALS; ANUS, IMPERFORATE; BODY PATTERNING; CELL COUNT; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CEREBRAL CORTEX; GENE DELETION; HEARING LOSS, SENSORINEURAL; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEUROGENESIS; NEUROGLIA; ORGAN SIZE; STEM CELLS; THUMB; TRANSCRIPTION FACTORS;

MUS;

EID: 84860741507     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.002873     Document Type: Article

References (110)

1. Al-Baradie, R., Yamada, K., St Hilaire, C., Chan, W. M., Andrews, C., McIntosh, N., Nakano, M., Martonyi, E. J., Raymond, W. R., Okumura, S. et al. (2002). Duane radial ray syndrome (Okihiro syndrome) maps to 20q13 and results from mutations in SALL4, a new member of the SAL family. Am. J. Hum. Genet. 71, 1195-1199. (Pubitemid 35305238)
2. Angevine, J. B., Jr and Sidman, R. L. (1961). Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766-768.
3. Arlotta, P., Molyneaux, B. J., Chen, J., Inoue, J., Kominami, R. and Macklis, J. D. (2005). Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207-221. (Pubitemid 40136579)
4. Arnold, S. E. (1999). Neurodevelopmental abnormalities in schizophrenia: insights from neuropathology. Dev. Psychopathol. 11, 439-456.
5. Attardo, A., Calegari, F., Haubensak, W., Wilsch-Brauninger, M. and Huttner, W. B. (2008). Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS ONE 3, e2388.
6. Avram, D., Fields, A., Pretty On Top, K., Nevrivy, D. J., Ishmael, J. E. and Leid, M. (2000). Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J. Biol. Chem. 275, 10315-10322.
7. Barembaum, M. and Bronner-Fraser, M. (2004). A novel spalt gene expressed in branchial arches affects the ability of cranial neural crest cells to populate sensory ganglia. Neuron Glia Biol. 1, 57-63.
8. Basson, M. and Horvitz, H. R. (1996). The Caenorhabditis elegans gene sem-4 controls neuronal and mesodermal cell development and encodes a zinc finger protein. Genes Dev. 10, 1953-1965. (Pubitemid 26281689)
9. Bedford, L., Walker, R., Kondo, T., van Cruchten, I., King, E. R. and Sablitzky, F. (2005). Id4 is required for the correct timing of neural differentiation. Dev. Biol. 280, 386-395. (Pubitemid 40692139)
10. Blanck, C., Kohlhase, J., Engels, S., Burfeind, P., Engel, W., Bottani, A., Patel, M. S., Kroes, H. Y. and Cobben, J. M. (2000). Three novel SALL1 mutations extend the mutational spectrum in Townes-Brocks syndrome. J. Med. Genet. 37, 303-307. (Pubitemid 30245939)
11. Borozdin, W., Steinmann, K., Albrecht, B., Bottani, A., Devriendt, K., Leipoldt, M. and Kohlhase, J. (2006). Detection of heterozygous SALL1 deletions by quantitative real time PCR proves the contribution of a SALL1 dosage effect in the pathogenesis of Townes-Brocks syndrome. Hum. Mutat. 27, 211-212.
12. Botzenhart, E. M., Green, A., Ilyina, H., Konig, R., Lowry, R. B., Lo, I. F., Shohat, M., Burke, L., McGaughran, J., Chafai, R. et al. (2005). SALL1 mutation analysis in Townes-Brocks syndrome: twelve novel mutations and expansion of the phenotype. Hum. Mutat. 26, 282.
13. Buck, A., Archangelo, L., Dixkens, C. and Kohlhase, J. (2000). Molecular cloning, chromosomal localization, and expression of the murine SALL1 ortholog Sall1. Cytogenet. Cell Genet. 89, 150-153.
14. Bulfone, A., Smiga, S. M., Shimamura, K., Peterson, A., Puelles, L. and Rubenstein, J. L. (1995). T-brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15, 63-78.
15. Cameron, T. H., Lachiewicz, A. M. and Aylsworth, A. S. (1991). Townes-Brocks syndrome in two mentally retarded youngsters. Am. J. Med. Genet. 41, 1-4.
16. Cantera, R., Luer, K., Rusten, T. E., Barrio, R., Kafatos, F. C. and Technau, G. M. (2002). Mutations in spalt cause a severe but reversible neurodegenerative phenotype in the embryonic central nervous system of Drosophila melanogaster. Development 129, 5577-5586. (Pubitemid 36054603)
17. Caviness, V. S., Jr (1982). Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res. 256, 293-302.
18. Caviness, V. S., Jr, Goto, T., Tarui, T., Takahashi, T., Bhide, P. G. and Nowakowski, R. S. (2003). Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb. Cortex 13, 592-598. (Pubitemid 36613166)
19. Cubelos, B., Sebastian-Serrano, A., Kim, S., Moreno-Ortiz, C., Redondo, J. M., Walsh, C. A. and Nieto, M. (2008). Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. Cereb. Cortex 18, 1758-1770. (Pubitemid 352019896)
20. de Celis, J. F., Barrio, R. and Kafatos, F. C. (1996). A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381, 421-424. (Pubitemid 26162731)
21. de Celis, J. F., Barrio, R. and Kafatos, F. C. (1999). Regulation of the spalt/spalt-related gene complex and its function during sensory organ development in the Drosophila thorax. Development 126, 2653-2662. (Pubitemid 29338627)
22. Elling, U., Klasen, C., Eisenberger, T., Anlag, K. and Treier, M. (2006). Murine inner cell mass-derived lineages depend on Sall4 function. Proc. Natl. Acad. Sci. USA 103, 16319-16324. (Pubitemid 44715194)
23. Engels, S., Kohlhase, J. and McGaughran, J. (2000). A SALL1 mutation causes a branchio-oto-renal syndrome-like phenotype. J. Med. Genet. 37, 458-460. (Pubitemid 30386741)
24. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251. (Pubitemid 40110787)
25. Farrell, E. R. and Munsterberg, A. E. (2000). csal1 is controlled by a combination of FGF and Wnt signals in developing limb buds. Dev. Biol. 225, 447-458.
26. Franklin, K. B. J. and Paxinos, G. (1997). The Mouse Brain in Stereotaxic Coordinates. New York: Academic Press.
27. Furuta, Y., Lagutin, O., Hogan, B. L. and Oliver, G. C. (2000). Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 26, 130-132. (Pubitemid 30158097)
28. Gillies, K. and Price, D. J. (1993). The fates of cells in the developing cerebral cortex of normal and methylazoxymethanol acetate-lesioned mice. Eur. J. Neurosci. 5, 73-84. (Pubitemid 23079501)
29. Gorski, J. A., Talley, T., Qiu, M., Puelles, L., Rubenstein, J. L. and Jones, K. R. (2002). Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci. 22, 6309-6314. (Pubitemid 35386383)
30. Gupta, A., Tsai, L. H. and Wynshaw-Boris, A. (2002). Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3, 342-355. (Pubitemid 34506716)
31. Hammerle, B. and Tejedor, F. J. (2002). A method for pulse and chase BrdU-labeling of early chick embryos. J. Neurosci. Methods 122, 59-64. (Pubitemid 36132168)
32. Handler, M., Yang, X. and Shen, J. (2000). Presenilin-1 regulates neuronal differentiation during neurogenesis. Development 127, 2593-2606. (Pubitemid 30426807)
33. Harrison, S. J., Nishinakamura, R. and Monaghan, A. P. (2008a). Sall1 regulates mitral cell development and olfactory nerve extension in the developing olfactory bulb. Cereb. Cortex 18, 1604-1617. (Pubitemid 351882039)
34. Harrison, S. J., Parrish, M. and Monaghan, A. P. (2008b). Sall3 is required for the terminal maturation of olfactory glomerular interneurons. J. Comp. Neurol. 507, 1780-1794. (Pubitemid 351468223)
35. Haubensak, W., Attardo, A., Denk, W. and Huttner, W. B. (2004). Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101, 3196-3201. (Pubitemid 38327757)
36. Haydar, T. F., Wang, F., Schwartz, M. L. and Rakic, P. (2000). Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 20, 5764-5774. (Pubitemid 30636905)
37. He, X., Treacy, M. N., Simmons, D. M., Ingraham, H. A., Swanson, L. W. and Rosenfeld, M. G. (1989). Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 340, 35-41.
38. Hevner, R. F. (2007). Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development. J. Neuropathol. Exp. Neurol. 66, 101-109.
39. Hevner, R. F., Shi, L., Justice, N., Hsueh, Y., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T. and Rubenstein, J. L. (2001). Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29, 353-366. (Pubitemid 32206476)
40. Inoue, S., Inoue, M., Fujimura, S. and Nishinakamura, R. (2010). A mouse line expressing Sall1-driven inducible Cre recombinase in the kidney mesenchyme. Genesis 48, 207-212.
41. Ishikiriyama, S., Kudoh, F., Shimojo, N., Iwai, J. and Inoue, T. (1996). Townes-Brocks syndrome associated with mental retardation. Am. J. Med. Genet. 61, 191-192.
42. Karantzali, E., Lekakis, V., Ioannou, M., Hadjimichael, C., Papamatheakis, J. and Kretsovali, A. (2011). Sall1 regulates embryonic stem cell differentiation in association with nanog. J. Biol. Chem. 286, 1037-1045.
43. Kawaguchi, A., Ogawa, M., Saito, K., Matsuzaki, F., Okano, H. and Miyata, T. (2004). Differential expression of Pax6 and Ngn2 between pair-generated cortical neurons. J. Neurosci. Res. 78, 784-795. (Pubitemid 39657566)
44. Kiefer, S. M., Ohlemiller, K. K., Yang, J., McDill, B. W., Kohlhase, J. and Rauchman, M. (2003). Expression of a truncated Sall1 transcriptional repressor is responsible for Townes-Brocks syndrome birth defects. Hum. Mol. Genet. 12, 2221-2227. (Pubitemid 37098991)
45. Kiefer, S. M., Robbins, L., Barina, A., Zhang, Z. and Rauchman, M. (2008). SALL1 truncated protein expression in Townes-Brocks syndrome leads to ectopic expression of downstream genes. Hum. Mutat. 29, 1133-1140.
46. Kohlhase, J., Wischermann, A., Reichenbach, H., Froster, U. and Engel, W. (1998). Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome. Nat. Genet. 18, 81-83. (Pubitemid 28027886)
47. Kohlhase, J., Hausmann, S., Stojmenovic, G., Dixkens, C., Bink, K., Schulz- Schaeffer, W., Altmann, M. and Engel, W. (1999a). SALL3, a new member of the human spalt-like gene family, maps to 18q23. Genomics 62, 216-222. (Pubitemid 30053937)
48. Kohlhase, J., Kohler, A., Jackle, H., Engel, W. and Stick, R. (1999b). Molecular cloning of a SALL1-related pseudogene and mapping to chromosome Xp11.2. Cytogenet. Cell Genet. 84, 31-34. (Pubitemid 29218920)
49. Kohlhase, J., Taschner, P. E., Burfeind, P., Pasche, B., Newman, B., Blanck, C., Breuning, M. H., ten Kate, L. P., Maaswinkel-Mooy, P., Mitulla, B. et al. (1999c). Molecular analysis of SALL1 mutations in Townes-Brocks syndrome. Am. J. Hum. Genet. 64, 435-445. (Pubitemid 129500526)
50. Kohlhase, J., Altmann, M., Archangelo, L., Dixkens, C. and Engel, W. (2000). Genomic cloning, chromosomal mapping, and expression analysis of msal-2. Mamm. Genome 11, 64-68. (Pubitemid 30033470)
51. Kohlhase, J., Heinrich, M., Liebers, M., Frohlich Archangelo, L., Reardon, W. and Kispert, A. (2002a). Cloning and expression analysis of SALL4, the murine homologue of the gene mutated in Okihiro syndrome. Cytogenet. Genome Res. 98, 274-277. (Pubitemid 37499859)
52. Kohlhase, J., Heinrich, M., Schubert, L., Liebers, M., Kispert, A., Laccone, F., Turnpenny, P., Winter, R. M. and Reardon, W. (2002b). Okihiro syndrome is caused by SALL4 mutations. Hum. Mol. Genet. 11, 2979-2987.
53. Kohlhase, J., Liebers, M., Backe, J., Baumann-Muller, A., Bembea, M., Destree, A., Gattas, M., Grussner, S., Muller, T., Mortier, G. et al. (2003). High incidence of the R276X SALL1 mutation in sporadic but not familial Townes-Brocks syndrome and report of the first familial case. J. Med. Genet. 40, e127.
54. Lee, M. K., Rebhun, L. I. and Frankfurter, A. (1990a). Posttranslational modification of class III beta-tubulin. Proc. Natl. Acad. Sci. USA 87, 7195-7199.
55. Lee, M. K., Tuttle, J. B., Rebhun, L. I., Cleveland, D. W. and Frankfurter, A. (1990b). The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton 17, 118-132. (Pubitemid 20372179)
56. Levers, T. E., Edgar, J. M. and Price, D. J. (2001). The fates of cells generated at the end of neurogenesis in developing mouse cortex. J. Neurobiol. 48, 265-277. (Pubitemid 32751480)
57. Li, D., Dower, K., Ma, Y., Tian, Y. and Benjamin, T. L. (2001). A tumor host range selection procedure identifies p150(sal2) as a target of polyoma virus large T antigen. Proc. Natl. Acad. Sci. USA 98, 14619-14624. (Pubitemid 33121441)
58. Lian, G. and Sheen, V. (2006). Cerebral developmental disorders. Curr. Opin. Pediatr. 18, 614-620. (Pubitemid 44747153)
59. Magdaleno, S., Jensen, P., Brumwell, C. L., Seal, A., Lehman, K., Asbury, A., Cheung, T., Cornelius, T., Batten, D. M., Eden, C. et al. (2006). BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol. 4, e86.
60. Marin, O. and Rubenstein, J. L. (2001). A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790. (Pubitemid 33674060)
61. Marlin, S., Blanchard, S., Slim, R., Lacombe, D., Denoyelle, F., Alessandri, J. L., Calzolari, E., Drouin-Garraud, V., Ferraz, F. G., Fourmaintraux, A. et al. (1999). Townes-Brocks syndrome: detection of a SALL1 mutation hot spot and evidence for a position effect in one patient. Hum. Mutat. 14, 377-386. (Pubitemid 29529542)
62. Martinez-Cerdeno, V., Noctor, S. C. and Kriegstein, A. R. (2006). The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb. Cortex 16 Suppl. 1, i152-i161.
63. McEvilly, R. J., de Diaz, M. O., Schonemann, M. D., Hooshmand, F. and Rosenfeld, M. G. (2002). Transcriptional regulation of cortical neuron migration by POU domain factors. Science 295, 1528-1532.
64. Menezes, J. R. and Luskin, M. B. (1994). Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 14, 5399-5416. (Pubitemid 24279060)
65. Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T. and Ogawa, M. (2004). Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145. (Pubitemid 39077437)
66. Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. and Gaiano, N. (2007). Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351-355. (Pubitemid 47443472)
67. Munji, R. N., Choe, Y., Li, G., Siegenthaler, J. A. and Pleasure, S. J. (2011). Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J. Neurosci. 31, 1676-1687.
68. Mutch, C. A., Schulte, J. D., Olson, E. and Chenn, A. (2010). Beta-catenin signaling negatively regulates intermediate progenitor population numbers in the developing cortex. PLoS ONE 5, e12376.
69. Nieto, M., Monuki, E. S., Tang, H., Imitola, J., Haubst, N., Khoury, S. J., Cunningham, J., Gotz, M. and Walsh, C. A. (2004). Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 479, 168-180. (Pubitemid 39314889)
70. Nishinakamura, R. (2008). Stem cells in the embryonic kidney. Kidney Int. 73, 913-917.
71. Nishinakamura, R., Matsumoto, Y., Nakao, K., Nakamura, K., Sato, A., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Scully, S., Lacey, D. L. et al. (2001). Murine homolog of SALL1 is essential for ureteric bud invasion in kidney development. Development 128, 3105-3115. (Pubitemid 32825755)
72. Nishinakamura, R., Uchiyama, Y., Sakaguchi, M. and Fujimura, S. (2011). Nephron progenitors in the metanephric mesenchyme. Pediatr. Nephrol. 26, 1463-1467.
73. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. and Kriegstein, A. R. (2001). Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720. (Pubitemid 32144516)
74. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. (Pubitemid 38129789)
75. Noctor, S. C., Martinez-Cerdeno, V. and Kriegstein, A. R. (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J. Comp. Neurol. 508, 28-44. (Pubitemid 351532566)
76. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H. and Mikoshiba, K. (1995). The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899-912.
77. Ott, T., Parrish, M., Bond, K., Schwaeger-Nickolenko, A. and Monaghan, A. (2001). A new member of the spalt-like zinc finger protein family, Msal3, is expressed in the CNS and sites of epithelial/mesenchymal interaction. Mech. Dev. 101, 203-207. (Pubitemid 32186327)
78. Parrish, M., Ott, T., Lance-Jones, C., Schuetz, G., Schwaeger-Nickolenko, A. and Monaghan, A. P. (2004). Loss of the Sall3 gene leads to palate deficiency, abnormalities in cranial nerves, and perinatal lethality. Mol. Cell. Biol. 24, 7102-7112. (Pubitemid 39014437)
79. Pilz, D., Stoodley, N. and Golden, J. A. (2002). Neuronal migration, cerebral cortical development, and cerebral cortical anomalies. J. Neuropathol. Exp. Neurol. 61, 1-11. (Pubitemid 34027716)
80. Polleux, F. and Lauder, J. M. (2004). Toward a developmental neurobiology of autism. Ment. Retard. Dev. Disabil. Res. Rev. 10, 303-317. (Pubitemid 40209463)
81. Pontious, A., Kowalczyk, T., Englund, C. and Hevner, R. F. (2008). Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24-32. (Pubitemid 350256680)
82. Price, D. J., Aslam, S., Tasker, L. and Gillies, K. (1997). Fates of the earliest generated cells in the developing murine neocortex. J. Comp. Neurol. 377, 414-422. (Pubitemid 27016648)
83. Rosner, B. S. (1970). Brain functions. Annu. Rev. Psychol. 21, 555-594.
84. Roy, K., Kuznicki, K., Wu, Q., Sun, Z., Bock, D., Schutz, G., Vranich, N. and Monaghan, A. P. (2004). The Tlx gene regulates the timing of neurogenesis in the cortex. J. Neurosci. 24, 8333-8345. (Pubitemid 39280812)
85. Rusten, T. E., Cantera, R., Urban, J., Technau, G., Kafatos, F. C. and Barrio, R. (2001). Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes. Development 128, 711-722. (Pubitemid 32229248)
86. Saffary, R. and Xie, Z. (2011). FMRP regulates the transition from radial glial cells to intermediate progenitor cells during neocortical development. J. Neurosci. 31, 1427-1439.
87. Sakaki-Yumoto, M., Kobayashi, C., Sato, A., Fujimura, S., Matsumoto, Y., Takasato, M., Kodama, T., Aburatani, H., Asashima, M., Yoshida, N. et al. (2006). The murine homolog of SALL4, a causative gene in Okihiro syndrome, is essential for embryonic stem cell proliferation, and cooperates with Sall1 in anorectal, heart, brain and kidney development. Development 133, 3005-3013. (Pubitemid 44314277)
88. Salerno, A., Kohlhase, J. and Kaplan, B. S. (2000). Townes-Brocks syndrome and renal dysplasia: a novel mutation in the SALL1 gene. Pediatr. Nephrol. 14, 25-28. (Pubitemid 30085338)
89. Sato, A., Kishida, S., Tanaka, T., Kikuchi, A., Kodama, T., Asashima, M. and Nishinakamura, R. (2004). Sall1, a causative gene for Townes-Brocks syndrome, enhances the canonical Wnt signaling by localizing to heterochromatin. Biochem. Biophys. Res. Commun. 319, 103-113. (Pubitemid 38670166)
90. Schiffmann, S. N., Bernier, B. and Goffinet, A. M. (1997). Reelin mRNA expression during mouse brain development. Eur. J. Neurosci. 9, 1055-1071. (Pubitemid 27226469)
91. Schwartzkroin, P. A. and Walsh, C. A. (2000). Cortical malformations and epilepsy. Ment. Retard. Dev. Disabil. Res. Rev. 6, 268-280.
92. Sessa, A., Mao, C. A., Hadjantonakis, A. K., Klein, W. H. and Broccoli, V. (2008). Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60, 56-69.
93. Sheppard, A. M. and Pearlman, A. L. (1997). Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J. Comp. Neurol. 378, 173-179. (Pubitemid 27057519)
94. Sheppard, A. M., Hamilton, S. K. and Pearlman, A. L. (1991). Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci. 11, 3928-3942.
95. Siegenthaler, J. A., Tremper-Wells, B. A. and Miller, M. W. (2008). Foxg1 haploinsufficiency reduces the population of cortical intermediate progenitor cells: effect of increased p21 expression. Cereb. Cortex. 18, 1865-1875. (Pubitemid 352019903)
96. Surka, W. S., Kohlhase, J., Neunert, C. E., Schneider, D. S. and Proud, V. K. (2001). Unique family with Townes-Brocks syndrome, SALL1 mutation, and cardiac defects. Am. J. Med. Genet. 102, 250-257. (Pubitemid 32730274)
97. Sweetman, D., Smith, T., Farrell, E. R., Chantry, A. and Munsterberg, A. (2003). The conserved glutamine-rich region of chick csal1 and csal3 mediates protein interactions with other spalt family members. Implications for Townes-Brocks syndrome. J. Biol. Chem. 278, 6560-6566. (Pubitemid 36800918)
98. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1994). Mode of cell proliferation in the developing mouse neocortex. Proc. Natl. Acad. Sci. USA 91, 375-379. (Pubitemid 24018707)
99. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1996a). Interkinetic and migratory behavior of a cohort of neocortical neurons arising in the early embryonic murine cerebral wall. J. Neurosci. 16, 5762-5776. (Pubitemid 26293399)
100. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1996b). The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci. 16, 6183-6196. (Pubitemid 26313993)
101. Takahashi, T., Goto, T., Miyama, S., Nowakowski, R. S. and Caviness, V. S., Jr (1999). Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J. Neurosci. 19, 10357-10371. (Pubitemid 30228043)
102. Tiveron, M. C., Rossel, M., Moepps, B., Zhang, Y. L., Seidenfaden, R., Favor, J., Konig, N. and Cremer, H. (2006). Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J. Neurosci. 26, 13273-13278. (Pubitemid 46011637)
103. Toker, A. S., Teng, Y., Ferreira, H. B., Emmons, S. W. and Chalfie, M. (2003). The Caenorhabditis elegans spalt-like gene sem-4 restricts touch cell fate by repressing the selector Hox gene egl-5 and the effector gene mec-3. Development 130, 3831-3840. (Pubitemid 37039087)
104. Townes, P. L. and Brocks, E. R. (1972). Hereditary syndrome of imperforate anus with hand, foot, and ear anomalies. J. Pediatr. 81, 321-326.
105. Walter, K. N., Greenhalgh, K. L., Newbury-Ecob, R. A. and Kohlhase, J. (2006). Mosaic trisomy 8 and Townes-Brocks syndrome due to a novel SALL1 mutation in the same patient. Am. J. Med. Genet. A 140, 649-651. (Pubitemid 43376306)
106. Wines-Samuelson, M., Handler, M. and Shen, J. (2005). Role of presenilin-1 in cortical lamination and survival of Cajal-Retzius neurons. Dev. Biol. 277, 332-346. (Pubitemid 40022955)
107. Wrobel, C. N., Mutch, C. A., Swaminathan, S., Taketo, M. M. and Chenn, A. (2007). Persistent expression of stabilized beta-catenin delays maturation of radial glial cells into intermediate progenitors. Dev. Biol. 309, 285-297. (Pubitemid 47361114)
108. Yamamoto, S., Yoshino, I., Shimazaki, T., Murohashi, M., Hevner, R. F., Lax, I., Okano, H., Shibuya, M., Schlessinger, J. and Gotoh, N. (2005). Essential role of Shp2-binding sites on FRS2alpha for corticogenesis and for FGF2-dependent proliferation of neural progenitor cells. Proc. Natl. Acad. Sci. USA 102, 15983-15988. (Pubitemid 41552854)
109. Yoon, K. J., Koo, B. K., Im, S. K., Jeong, H. W., Ghim, J., Kwon, M. C., Moon, J. S., Miyata, T. and Kong, Y. Y. (2008). Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58, 519-531. (Pubitemid 351672356)
110. Yuri, S., Fujimura, S., Nimura, K., Takeda, N., Toyooka, Y., Fujimura, Y., Aburatani, H., Ura, K., Koseki, H., Niwa, H. and Nishinakamura, R. (2009). Sall4 is essential for stabilization, but not for pluripotency, of embryonic stem cells by repressing aberrant trophectoderm gene expression. Stem Cells 27, 796-805.